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Link to original content: https://pubmed.ncbi.nlm.nih.gov/28839251
Odours of Plasmodium falciparum-infected participants influence mosquito-host interactions - PubMed Skip to main page content
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. 2017 Aug 24;7(1):9283.
doi: 10.1038/s41598-017-08978-9.

Odours of Plasmodium falciparum-infected participants influence mosquito-host interactions

Jetske G de Boer  1   2 , Ailie Robinson  3 , Stephen J Powers  4 , Saskia L G E Burgers  5 , John C Caulfield  6 , Michael A Birkett  6 , Renate C Smallegange  7   3 , Perry J J van Genderen  8 , Teun Bousema  9 , Robert W Sauerwein  9 , John A Pickett  6 , Willem Takken  7 , James G Logan  3
Affiliations

Odours of Plasmodium falciparum-infected participants influence mosquito-host interactions

Jetske G de Boer et al. Sci Rep. .

Abstract

Malaria parasites are thought to influence mosquito attraction to human hosts, a phenomenon that may enhance parasite transmission. This is likely mediated by alterations in host odour because of its importance in mosquito host-searching behaviour. Here, we report that the human skin odour profile is affected by malaria infection. We compared the chemical composition and attractiveness to Anopheles coluzzii mosquitoes of skin odours from participants that were infected by Controlled Human Malaria Infection with Plasmodium falciparum. Skin odour composition differed between parasitologically negative and positive samples, with positive samples collected on average two days after parasites emerged from the liver into the blood, being associated with low densities of asexual parasites and the absence of gametocytes. We found a significant reduction in mosquito attraction to skin odour during infection for one experiment, but not in a second experiment, possibly due to differences in parasite strain. However, it does raise the possibility that infection can affect mosquito behaviour. Indeed, several volatile compounds were identified that can influence mosquito behaviour, including 2- and 3-methylbutanal, 3-hydroxy-2-butanone, and 6-methyl-5-hepten-2-one. To better understand the impact of our findings on Plasmodium transmission, controlled studies are needed in participants with gametocytes and higher parasite densities.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1
Effect of Plasmodium falciparum infection on the composition of human skin odour. Canonical variates plots of (a) CHMI1 and (b) CHMI2 chemistry data (Porapak samples) are grouped by parasitological status (irrespective of sampling timepoint), and (c) grouped by P. falciparum strain within samples of CHMI2 (numbers of samples per group with number of individuals in brackets). CHMI1 and CHMI2 refer to two controlled human malaria infection studies in which our samples were collected. Participants were infected with P. falciparum strain NF54 in CHMI1, and with strains NF135.C8 or NF166.C10 in CHMI2. Samples are positioned by scores (indicated by + symbols) on canonical variate axes relative to the presence and quantity of compounds contributing to these axes. The percentage of possible discrimination accounted for is included in the axes labels. Circles represent 95% confidence intervals around means (x symbols) of scores. Controls of empty bag sampling and the diethyl ether used during sample elution were analysed and included as control groups but excluded from figures to maintain clarity. Parasitological status was defined by qPCR-testing on the same day. In panel C, samples collected during and after infection are included from participants that became parasitologically positive at least once during infection.
Figure 2
Figure 2
Effect of Plasmodium falciparum infection on levels of specific human volatile compounds. Compounds of interest identified in samples of (a) CHMI1 and (b) CHMI2 were analysed by temporal parasitological status [Before: sampling timepoint before malaria challenge; During: 6–8 days post malaria challenge, with (−) and (+) referring to parasitological status, measured by qPCR; After: after antimalarial treatment; Control: headspace collected from empty control bags]. Back-transformed predicted means (REML) are shown (amounts in ng collected over 100 min. for Porapak – left two panels, amounts in peak area units*1000 collected over 20 min for Tenax – right three panels). For predicted means (log transformation) with standard errors, see Supplementary Fig. S4 and Tables S1 and S2 for pairwise SEDs. In CHMI2, the number of Porapak and Tenax samples varied as indicated in the figure legend; exact n given in Table 2, and Fig. S4. RI 1095 (CHMI1) and 1-Dodecene, dodecanal, methyl dodecanoate and RI 1416 (CHMI2) each co-eluted with another unidentified compound and hence their quantities are difficult to obtain accurately. Differences in amounts observed in temporal P. falciparum infection categories can therefore not be attributed with absolute certainty to these compounds.
Figure 3
Figure 3
Choice of Anopheles coluzzii for cotton pads worn by participants in two Controlled Human Malaria Infection studies. Proportions of mosquitoes trapped in the two traps of the olfactometer are plotted at three sampling time points relative to P. falciparum infection: Before, During and After, with parasitological status by qPCR during infection indicated by (−) for qPCR-negatives and (+) for qPCR-positives. Control traps contained a cotton pad with NH3. Back-transformed predicted mean proportions of mosquitoes are plotted, from the GLMMs including temporal P. falciparum infection as a fixed effect term and participant as a random effect term. Numbers in bars represent the number of cotton pad samples tested in each group (N = 6 individuals in CHMI1, N = 9 individuals in CHMI2). P-values are given for the effect of temporal P. falciparum infection within each CHMI study, with significant pairwise differences within CHMI1 indicated by different letters above bars, tested at the logistic scale (P < 0.05). For predicted means (logistic transformation) with standard errors, see Fig. S6, and for pairwise t-probabilities of CHMI1, see Table S3.
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